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Avian Malaria Vectors in Host-Seeking Behaviour
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Vector-borne infectious diseases (e.g., malaria, dengue fever, and yellow fever) result from a parasite transmitted to humans and other animals by blood-feeding arthropods. They are major contributors to the global disease burden, as they account for nearly a fifth of all infectious diseases worldwide. The interaction between vectors and their hosts plays a key role driving vector-borne disease transmission.

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Table of Contents

    1. Avian Haemosporidians and Their Vectors

    Vector-borne diseases (e.g., malaria, yellow fever, dengue fever) are major contributors to the global disease burden. Malaria is probably the most deathly and prevalent parasitic disease in the history of mankind. Indeed, it is estimated that about 150–300 million people have died from the effects of malaria during the past 100 years [1]. In 2020, there were an estimated 241 million cases of malaria worldwide, and 40% of the world’s population still lives in areas where malaria is transmitted [2].
    However, the systematicity and diversity of malaria parasites is much larger and not restricted to human parasites. These protozoan intracellular pathogens belong to order Haemosporidia, with numerous species from 15 genera infecting reptiles, birds, and mammals all around the world [3]. Avian haemosporidians are the largest group among all the haemosporidians infecting vertebrates by number of described species [4][5]. So far, more than 4600 parasite lineages from the genera Plasmodium, Haemoproteus, Leucocytozoon, and Fallisia have been described in more than 1900 avian species (MALAVI database version 2.5.2, December 2021 [6]). Moreover, new lineages are reported every year revealing the remaining unexplored genetic diversity of these parasites, mainly in the tropics [7][8][9][10]. These blood parasites may provoke detrimental effects on their avian host by reducing their survival [11][12][13], minimizing their reproductive success [14][15] and provoking tissue damage [16], hence reducing bird populations and eventually being responsible for population extinctions following the introduction of exotic haemosporidian parasites beyond their natural range [17]. They are globally distributed, infecting individuals representing most bird clades in all the continents except Antarctica [18], thus constituting an excellent model for the study of vector-host–parasite interactions [4].
    The term “malaria parasites” has been a debated issue among parasitologists, ecologists, and evolutionary researchers [19][20]. The controversy lies from the incomplete knowledge of the phylogenetic relationships and pathogenicity of non-human malaria parasites [21]. Although some similarities can be observed in the life cycles of Plasmodium, Haemoproteus, and Leucocytozoon, they still have some differences in vectors, life cycles, and epidemiology [22]. Therefore, traditional taxonomists and parasitologists only accept Plasmodium species as being the true malaria parasites [4]. However, based on molecular genetic studies describing the phylogeny of the group, other authors also include other genera (i.e., Haemoproteus, Leucocytozoon) among the term “malaria parasites” [19]. Haemosporidians are obligate heteroxenous parasites, with some parts of their life cycle developing within their blood-feeding arthropod vectors (sexual reproduction), whereas some stages occur within their vertebrate hosts (asexual reproduction). After the inoculation of haemosporidian sporozoites from an infective vector, the parasites may either complete their life cycle in a susceptible host or abort their development in a non-susceptible host unable to develop infective stages (gametocytes) to reach a new host [5].
    The infection starts with the bite of a female dipteran insect transmitting infective stages (sporozoites) from its saliva into the blood stream of the avian host while taking a blood meal. Afterwards, the sporozoites initiate the development of exoerythrocytic meronts in the endothelial cells of many organs and tissues. Meronts undergo asexual divisions in these cells and form merozoites for a minimum of two generations before the parasite produce merozoites capable to infect erythrocytes. This part of the life cycle before the development of merozoites that are able of invading blood cells is called the prepatent period (10–14 days). This extraerythrocytic stage is essential to enhance the initial infectious source. The breakage of host endothelial cells releases merozoites into the blood stream, which may result in (i) additional infection of reticuloendothelial cells; or (ii) invasion of red blood cells giving rise to gametocytes (macrogametocytes and microgametocytes), which are infective to vectors. Gametocytes remain inside erythrocytes until ingestion by a dipteran insect in which the sexual process and sporogony take place. The inoculation of infective sporozoites will initiate new infections in vertebrate hosts [4][5][22].
    The patent period of infection (interval during which parasites can be found in the blood stream) begins when parasites enter circulating erythrocytes, and encompasses different phases: (a) the acute stage, the initial phase when intensity of parasitaemia increases; (b) crisis, when parasitaemia reaches a maximum; and (c) the chronic phase, where the parasitaemia decreases and stabilizes at low levels. In haemosporidian infection, however, the chronic phase may be followed by a latent stage of infection, where parasites are absent in the blood stream but persist in internal organs. These tissue stages may initiate asexual replications leading to relapses and temporary increases of parasitaemia [4][5][22]. It has been shown that avian malaria Plasmodium relictum reacts to mosquito bites by increasing its overall parasitaemia in the blood during the chronic stage of the infection, which may result in enhanced probability of infection to mosquitoes and thus increased transmission rates [23].
    To date, only species of blood-sucking dipteran insects (Diptera) have been described as vectors for haemosporidian parasites [24]. Culicidae mosquitoes from five genera (Anopheles, Culex, Aedes, Culiseta, Coquillettidia) are capable of transmitting avian Plasmodium parasites [24]. Other mosquito genera such as Mansonia and Lutzia have been found to carry Plasmodium lineages [25][26], but their competence in successfully transmitting malaria parasites still needs experimental confirmation (e.g., visual and molecular identification of sporozoites in salivary glands of these mosquitoes). Within the genus Haemoproteus, biting midges (mostly of the genus Culicoides, Ceratopogonidae) transmit parasites of the subgenus Parahaemoproteus, whereas parasites from subgenus Haemoproteus are vectored by louse flies (Hippoboscidae) [24]. For the genus Leucocytozoon, it is generally accepted that parasite species from subgenus Leucocytozoon are transmitted by black flies (Simuliidae), while ceratopogonid flies are responsible for the transmission of the only species of Akiba subgenus infecting birds (A. caulleryi) [27]. The only species of the genus Fallisia infecting birds is supposed to be transmitted by culicine mosquitoes [28], but this requires verification.

    2. Cues Followed by Haemosporidian Vectors to Locate Their Hosts

    Vector control is a crucial strategy for global malaria control in preventing infection and reducing disease transmission [29]. Although the contact between hosts and vectors may play a key role driving vector-borne disease transmission, vector density has been largely studied to analyse transmission risk, while host–vector contact dynamics, including host-seeking behaviour, have received less attention [30]. Historically, avian models have provided important insights to explain variations in disease risk, thus enhancing the knowledge on ecological and evolutionary processes ruling host–parasite interactions [31]. Identifying factors governing host selection by blood-feeding insects is essential to understand the transmission dynamics of vector-borne diseases [32]. Arthropod vectors may use a number of physical and chemical stimuli emitted by vertebrate hosts to detect their blood meal sources, including acoustic, visual, olfactory, moisture, and thermal cues (Figure 1) [33][34][35] (Table 1).
    Figure 1. The sensory cues used by mosquitoes to detect their prey are distance-dependent. Mosquitoes follow a combination of cues to detect their potential hosts according to their proximity. Mosquitoes at larger distances can detect odours and CO2 exhaled from host’s breath, whereas vectors use body temperature and visual stimuli to locate their hosts at closer ranges. Adapted from [34][35].
    Table 1. Summary of studies reporting increased (+), decreased (−), or neutral (0) attraction of avian haemosporidian vectors towards different stimuli.

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      Marzal, A.; Magallanes, S.; Batanete, L.G. Avian Malaria Vectors in Host-Seeking Behaviour. Encyclopedia. Available online: https://encyclopedia.pub/entry/23138 (accessed on 01 December 2022).
      Marzal A, Magallanes S, Batanete LG. Avian Malaria Vectors in Host-Seeking Behaviour. Encyclopedia. Available at: https://encyclopedia.pub/entry/23138. Accessed December 01, 2022.
      Marzal, Alfonso, Sergio Magallanes, Luz Garcia-Longoria Batanete. "Avian Malaria Vectors in Host-Seeking Behaviour," Encyclopedia, https://encyclopedia.pub/entry/23138 (accessed December 01, 2022).
      Marzal, A., Magallanes, S., & Batanete, L.G. (2022, May 19). Avian Malaria Vectors in Host-Seeking Behaviour. In Encyclopedia. https://encyclopedia.pub/entry/23138
      Marzal, Alfonso, et al. ''Avian Malaria Vectors in Host-Seeking Behaviour.'' Encyclopedia. Web. 19 May, 2022.
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